Bottom Line:
However, virtually nothing is known about the impact of the voluntary generation of compassion on this network.These results support the role of the limbic circuitry in emotion sharing.Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.

Affiliation: University of Wisconsin, Madison, Wisconsin, United States of America. alutz@wisc.edu

ABSTRACTRecent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated insula and anterior cingulate cortices in the empathic response to another's pain. However, virtually nothing is known about the impact of the voluntary generation of compassion on this network. To investigate these questions we assessed brain activity using fMRI while novice and expert meditation practitioners generated a loving-kindness-compassion meditation state. To probe affective reactivity, we presented emotional and neutral sounds during the meditation and comparison periods. Our main hypothesis was that the concern for others cultivated during this form of meditation enhances affective processing, in particular in response to sounds of distress, and that this response to emotional sounds is modulated by the degree of meditation training. The presentation of the emotional sounds was associated with increased pupil diameter and activation of limbic regions (insula and cingulate cortices) during meditation (versus rest). During meditation, activation in insula was greater during presentation of negative sounds than positive or neutral sounds in expert than it was in novice meditators. The strength of activation in insula was also associated with self-reported intensity of the meditation for both groups. These results support the role of the limbic circuitry in emotion sharing. The comparison between meditation vs. rest states between experts and novices also showed increased activation in amygdala, right temporo-parietal junction (TPJ), and right posterior superior temporal sulcus (pSTS) in response to all sounds, suggesting, greater detection of the emotional sounds, and enhanced mentation in response to emotional human vocalizations for experts than novices during meditation. Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.

pone-0001897-g003: State by Group Interaction: A.(Amyg.) stands for amygdala (y = −5, color codes: orange, p<2.10ˆ-3, yellow, p<5.10ˆ-4). B. Impulse response in (Amyg.) for 15 experts (red) and for 15 novices (blue) during rest (dashed line) and compassion (full line). C–D. Same as A–B in TPJ; y = −61. E. Side by state effect and side by state by group effect in TPJ on the average impulse response between meditation and rest; experts are in red, novices in blue.

Mentions:
There were no Group-by-Valence or State-by-Valence interactions. Voxelwise analysis of group-by-state interactions showed experts to have had considerably stronger activation in components of the posterior part of this network (right TPJ, right pSTS, Prc./PCC) (Figs. 3.C–D), in the right inferior frontal gyrus (IFG), bilateral amygdalae (Figs. 3.A–B) and in two motor regions (pre-central gyri and post. medial frontal cortex, BA6) (Table 5). The magnitude of the group-by-state interaction was driven by the BOLD response of experts, who showed a negative average impulse response to the sounds at rest (Figs. 4.A and 4.E) but a positive response in these regions during meditation (Figs. 4.B and 4.F) in right TPJ, right IFG, Prc./PCC and mPFC. Novices and experts showed similar positive activation in the auditory cortex during both rest and meditation, indicating, as expected, sensory correlates of the auditory sounds (Figs. 4.E–H). These group differences were also highlighted in patterns of asymmetric BOLD response in the TPJ where experts showed a strong right-sided activation bias while novices showed virtually no activation difference to the emotional sounds in this region during meditation vs. rest (Fig. 3.E, Table 6).

pone-0001897-g003: State by Group Interaction: A.(Amyg.) stands for amygdala (y = −5, color codes: orange, p<2.10ˆ-3, yellow, p<5.10ˆ-4). B. Impulse response in (Amyg.) for 15 experts (red) and for 15 novices (blue) during rest (dashed line) and compassion (full line). C–D. Same as A–B in TPJ; y = −61. E. Side by state effect and side by state by group effect in TPJ on the average impulse response between meditation and rest; experts are in red, novices in blue.

Mentions:
There were no Group-by-Valence or State-by-Valence interactions. Voxelwise analysis of group-by-state interactions showed experts to have had considerably stronger activation in components of the posterior part of this network (right TPJ, right pSTS, Prc./PCC) (Figs. 3.C–D), in the right inferior frontal gyrus (IFG), bilateral amygdalae (Figs. 3.A–B) and in two motor regions (pre-central gyri and post. medial frontal cortex, BA6) (Table 5). The magnitude of the group-by-state interaction was driven by the BOLD response of experts, who showed a negative average impulse response to the sounds at rest (Figs. 4.A and 4.E) but a positive response in these regions during meditation (Figs. 4.B and 4.F) in right TPJ, right IFG, Prc./PCC and mPFC. Novices and experts showed similar positive activation in the auditory cortex during both rest and meditation, indicating, as expected, sensory correlates of the auditory sounds (Figs. 4.E–H). These group differences were also highlighted in patterns of asymmetric BOLD response in the TPJ where experts showed a strong right-sided activation bias while novices showed virtually no activation difference to the emotional sounds in this region during meditation vs. rest (Fig. 3.E, Table 6).

Bottom Line:
However, virtually nothing is known about the impact of the voluntary generation of compassion on this network.These results support the role of the limbic circuitry in emotion sharing.Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.

Affiliation:
University of Wisconsin, Madison, Wisconsin, United States of America. alutz@wisc.edu

ABSTRACTRecent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated insula and anterior cingulate cortices in the empathic response to another's pain. However, virtually nothing is known about the impact of the voluntary generation of compassion on this network. To investigate these questions we assessed brain activity using fMRI while novice and expert meditation practitioners generated a loving-kindness-compassion meditation state. To probe affective reactivity, we presented emotional and neutral sounds during the meditation and comparison periods. Our main hypothesis was that the concern for others cultivated during this form of meditation enhances affective processing, in particular in response to sounds of distress, and that this response to emotional sounds is modulated by the degree of meditation training. The presentation of the emotional sounds was associated with increased pupil diameter and activation of limbic regions (insula and cingulate cortices) during meditation (versus rest). During meditation, activation in insula was greater during presentation of negative sounds than positive or neutral sounds in expert than it was in novice meditators. The strength of activation in insula was also associated with self-reported intensity of the meditation for both groups. These results support the role of the limbic circuitry in emotion sharing. The comparison between meditation vs. rest states between experts and novices also showed increased activation in amygdala, right temporo-parietal junction (TPJ), and right posterior superior temporal sulcus (pSTS) in response to all sounds, suggesting, greater detection of the emotional sounds, and enhanced mentation in response to emotional human vocalizations for experts than novices during meditation. Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.